Coordinated assembly and release of adhesions builds apical junctional belts during de novo polarisation of an epithelial tube

Abstract

Using the zebrafish neural tube as a model, we uncover the in vivo mechanisms allowing the generation of two opposing apical epithelial surfaces within the centre of an initially unpolarised, solid organ. We show that Mpp5a and Rab11a play a dual role in coordinating the generation of ipsilateral junctional belts whilst simultaneously releasing contralateral adhesions across the centre of the tissue. We show that Mpp5a- and Rab11a-mediated resolution of cell-cell adhesions are both necessary for midline lumen opening and contribute to later maintenance of epithelial organisation. We propose that these roles for both Mpp5a and Rab11a operate through the transmembrane protein Crumbs. In light of a recent conflicting publication, we also clarify that the junction-remodelling role of Mpp5a is not specific to dividing cells.

The neurogenic fate of the hindbrain boundaries relies on Notch3-dependent asymmetric cell divisions

“…The following references appear in the supplemental information: Kidwell et al (2018); Symonds et al (2020).…”

The neurogenic fate of the hindbrain boundaries relies on Notch-dependent asymmetric cell divisions

“…(O, P) Double immunostaining of wild-type embryos at 30 hpf with Taz and ZO-1. Taz is expressed in the ventricular domain of the boundaries (Voltes et al, 2019); ZO-1 labelling allows the larger apical feet of boundary cells to be visualized (Symonds et al, 2020). Q-R) Transverse views of the Tg[BCP:H2AmCherry;4xGTIIC:d2GFP] embryos showing that mCherry-boundary cells display Yap/Taz-TEAD-activity at 33 hpf (Q-Q’) and 48 hpf (R-R’).…”

E‐cadherin mediates apical membrane initiation site localisation during de novo polarisation of epithelial cavities

“…For example, Cingulin is a tight junctional protein that has been shown to bind both to the midbody and to FIP5, which is important for the apical targeting of vesicles containing apical proteins (Mangan et al , 2016). During zebrafish neural rod development, cell adhesion and cell division align to allow an organised structure to arise from dynamically reorganising cells (Symonds & Buckley et al , 2020) and loss of N‐cadherin results in mis‐oriented cell divisions and a disrupted apical domain (Žigman et al , 2011). Once apical proteins fuse with the apical membrane, proteins associated with junctions such as Cadherin, PAR‐3 and ZO‐1 are then cleared from the apical surface and instead form the apical‐lateral junctions, as demonstrated in several different epithelial systems (Morais‐de‐Sa et al , 2010; Symonds & Buckley et al , 2020; Kim et al , 2021).…”

“…This suggests that, whilst cell division is undoubtably a dominant mechanism, there must be another overlying mechanism driving AMIS localisation during de novo polarisation. The earliest indication of midline positioning in the zebrafish neural rod is the central accumulation of the junctional scaffolding protein Pard3 (PAR‐3) and the adhesion protein N‐cadherin (Buckley et al , 2013; Symonds & Buckley et al , 2020). This led us to hypothesise that cell–cell adhesions could direct the site for AMIS localisation during de novo polarisation.…”